Elucidating the metabolism of members of the Asgard archaea to help updating models on the origin of the eukaryotic cell

The origin of the eukaryotic cell represents one of the most fundamental mysteries in the evolution of cellular life on Earth. Already in the beginning of the 20th century, several researchers and cell biologists noticed the resemblance of mitochondria and chloroplasts to free-living bacteria, an observation that shaped the basis for various subsequently formulated endosymbiotic theories, which suggest that eukaryotic organelles are derived from bacterial symbionts. Throughout the years, various detailed models have been proposed to account for the partners involved as well as the processes underlying this symbiosis (Lopez-Garcia and Moreira, 2015; Lopez-Garcia et al., 2017; Martin et al., 2017). Yet, while the identity of the ancestors of mitochondria and chloroplasts could be ascribed to alpha-proteobacteria and cyanobacteria, respectively, the nature of the host cell remained an enigma for several decades.

Share

Copy the link

Only recently has the discovery of novel archaeal lineages enabled through the use of metagenomics, i.e. the sequencing of DNA directly isolated from environmental samples, helped to shed more light onto the elusive host of eukaryotic cells. In particular, such a sequencing approach has allowed the reconstruction of genomes of a so far uncultivated group of archaea, which was collectively referred to as the Asgard archaea and comprises lineages such as the Lokiarchaeota, Thorarchaeota, Heimdallarchaeota and Odinarchaeta (Spang et al., 2015; Zaremba-Niedzwiedzka et al., 2017). Organisms belonging to these lineages encode various proteins and protein domains that have previously only been found in eukaryotes but are generally absent from genomes of bacteria and other archaea. Furthermore, the placement of these lineages in the tree of life suggested that they represent the closest sister group of eukaryotes. Altogether, this research indicated, that the enigmatic host cell might have been an archaeon related to Asgard archaea.

But what was the driving force underlying the symbiosis between such an archaeal ancestor and the bacterial symbiont? Several previously formulated hypotheses, such as the hydrogen or symbiogenetic theory (Martin and Müller, 1998; Moreira and Lopez-Garcia, 1998) suggested that a metabolic interaction may have been central to eukaryogenesis. These scenarios are based upon the notion, that metabolic symbioses, i.e. syntrophic interactions between unrelated organisms, are common in nature and can lead to close associations based on the exchange of substrates or the direct transfer of electrons. For example, an interaction based on electron transfer characterizes various so called ANME consortia (McGlynn et al., 2015; Wegener et al., 2015), which consist of anaerobic methane oxidizing archaea and bacterial partners, the latter of which metabolize electrons generated by the archaea and thereby render growth on methane metabolically feasible.

However, given that previous scenarios were based on limited knowledge of the nature of the archaeal ancestor of eukaryotes, we decided to investigate the metabolic repertoire of extant members of the Asgard archaea and based on this knowledge formulate an updated model on the origin of the eukaryotic cell, which we refer to as the “Reverse flow model” (https://www.nature.com/articles/s41564-019-0406-9). In this model, we suggest that the archaeal ancestor of eukaryotes may have consumed organic substrates and generated reducing equivalents, that were metabolized syntrophically by the bacterial partner organism. The eukaryotic-like signature proteins of Asgard archaea, which among others are related to cytoskeleton and trafficking machinery proteins, may have played a role in establishing a tighter interaction between the archaeal host and bacterial partner(s). Over time, such a symbiotic interaction may have evolved into a more intricate relationship and ultimately into the loss of the integrity of the original partners.

While we think that this scenario seems best compatible with current knowledge on the genome repertoire of members of the Asgard archaea, the further characterization of this diverse archaeal lineage will be crucial to refine the steps that have led to the origin of the first eukaryotes more than 2 billion years ago. At the same time, the herein inferred metabolic features provide important information that can guide the targeted enrichment of Asgard archaea. Clearly, the ability to grow these archaea in a laboratory setting will be essential for characterizing the physiology and cell biology of these archaea and testing hypotheses on their ecology and interaction with other organism groups.

This community is not edited and does not necessarily reflect the views of Nature Research. Nature Research makes no representations, warranties or guarantees, whether express or implied, that the content on this community is accurate, complete or up to date, and to the fullest extent permitted by law all liability is excluded.

Please sign in or register for FREE

Sign in to Nature Research Microbiology Community

Register to Nature Research Microbiology Community

The Nature Research Microbiology Community provides a forum for the sharing and discussion of ideas and opinions about microbiology. Through posts, discussion, image and video content, the community space can be used by members to communicate with each other, and with editors, about topics ranging from the science itself through to policy, society and day to day life. It is also a place to learn more about the activities of Nature Microbiology's editors and the policies and practices of the journal.